Download Bioenergetic Prediction of Climate Change

INTEGR. COMP. BIOL., 44:152–162 (2004)
Bioenergetic Prediction of Climate Change Impacts on Northern Mammals1
MURRAY M. HUMPHRIES,2,* JAMES UMBANHOWAR,†
AND
KEVIN S. MCCANN†
*Department of Natural Resource Sciences, Macdonald Campus, McGill University, 21,111 Lakeshore Road,
Ste-Anne-de-Bellevue, Quebec H9X 3V9, Canada
†Department of Zoology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
SYNOPSIS. Climate change will likely alter the distribution and abundance of northern mammals through
a combination of direct, abiotic effects (e.g., changes in temperature and precipitation) and indirect, biotic
effects (e.g., changes in the abundance of resources, competitors, and predators). Bioenergetic approaches
are ideally suited to predicting the impacts of climate change because individual energy budgets integrate
biotic and abiotic influences, and translate individual function into population and community outcomes. In
this review, we illustrate how bioenergetics can be used to predict the regional biodiversity, species range
limits, and community trophic organization of mammals under future climate scenarios. Although reliable
prediction of climate change impacts for particular species requires better data and theory on the physiological ecology of northern mammals, two robust hypotheses emerge from the bioenergetic approaches
presented here. First, the impacts of climate change in northern regions will be shaped by the appearance
of new species at least as much as by the disappearance of current species. Second, seasonally inactive
mammal species (e.g., hibernators), which are largely absent from the Canadian arctic at present, should
undergo substantial increases in abundance and distribution in response to climate change, probably at the
expense of continuously active mammals already present in the arctic.
INTRODUCTION
Bioenergetics describes the process by which food
resources are acquired, assimilated, and allocated
among maintenance, growth, and reproduction
(McNab, 2001). Accordingly, energetics serves as a
primary linkage between physiological processes of
individuals and the ecological patterns of populations
(Odum, 1963; Yodzis and Innes, 1992). By definition,
energetics focuses on the acquisition and allocation of
energy, and indeed, energy is widely accepted as the
primary limiting resource in most terrestrial systems
(McNab, 2001). Additionally, many of the general
principles employed in energetics (e.g., mass-balance
equations, trophic linkages) are equally applicable to
interactions limited by other resources.
The earth is in the midst of a pronounced warming
trend, and more substantial changes in temperature,
precipitation, ocean circulation, and ice dynamics are
expected during the next century (Houghton et al.,
2001). As evidence for widespread biological impacts
of recent climate change accumulates (Parmesan and
Yohe, 2003; Root et al., 2003), there is growing demand to anticipate the future responses of plant and
animal populations to ongoing environmental change
(Ludwig et al., 2001). The ability of biologists to anticipate these biotic responses is limited to some degree by lingering uncertainty about the underlying
causes of climate change and how regional climates
will be affected by the complex, interactive effects of
global changes in temperature, precipitation, and circulation patterns (Houghton et al., 2001). Neverthe-
less, arguably the greater uncertainty is how biological
communities will respond to even the most robust and
widely accepted components of projected climate
change. Besides, as we hope to illustrate in this review,
temperature and seasonality are so fundamental to our
understanding of the organization of biological communities, that further investigation of their effects can
provide biological insights quite independent of issues
related to climate change.
The impacts of climate change on animal populations are likely to include both direct and indirect effects. For the purposes of this review, we consider direct effects of climate change to be those resulting
from changes to a population’s abiotic environment.
Hence, direct effects of climate change on animal populations might include altered mortality or reproductive rates resulting from changes in ambient temperature, the frequency and severity of extreme weather
events, the depth and duration of snow and ice cover,
and the availability of surface water. In contrast, we
consider indirect effects to include those resulting from
changes in a population’s biotic environment, specifically the distribution and abundance of their resources,
predators, and competitors. Because patterns of individual energy intake and expenditure represent the
point of integration for abiotic and biotic influences,
energetic approaches are uniquely suited to prediction
of both direct and indirect effects of climate change.
In the current review, we illustrate three ways in
which energetic approaches can be used to predict the
impacts of climate change on mammal populations in
northern environments. The first of these relies on biogeographical patterns of environmental energy availability and biodiversity to infer how climate change
will impact regional species diversity. The second focuses on species that routinely experience seasonal pe-
1 From the Symposium Biology of the Canadian Arctic: A Crucible for Change in the 21st Century presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8
January 2003, at Toronto, Canada.
2 E-mail: [email protected]
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MAMMAL ENERGETICS
riods of negative energy balance, and quantifies direct
effects of climate on the duration and severity of these
seasonal energetic bottlenecks to predict how climate
change will modify species range limits. The third uses
trophic energy flow models to predict the combined
impacts of direct and indirect effects of climate change
on simplified northern food webs. These same approaches could be applied to terrestrial vertebrates other than mammals, but we do not do so here because
amphibians and reptiles are generally absent or present
at low densities in subarctic and arctic regions, whereas birds are abundant, but their local dynamics are
complicated by migration and allochthonous energy
inputs (Jefferies and Rockwell, 2004; Gauthier and
Bêty, 2004). Furthermore, by focussing on energetics
in this review, we do not mean to imply that nonenergetic factors, such as disease, stress, or abiotic
habitat modification, will be unimportant in shaping
wildlife responses to climate change. Instead, we view
energetics as simply a uniquely appropriate starting
point for predicting climate change impacts, establishing an ‘‘all-else-being-equal’’ platform of expected
change that studies of other non-energetic factors will
surely modify.
I. SPECIES-ENERGY PATTERNS AND REGIONAL
DIVERSITY
Regional biodiversity varies dramatically with latitude (MacArthur, 1965; Rosenzweig, 1995). Animal
and plant diversity tends to increase from the equator
to the tropics, then decline precipitously from tropical
to polar latitudes (Rosenzweig, 1995). According to
the species-energy hypothesis (Currie, 1991), variation
in radiant energy flux per unit area is the primary determinant of the tropical-polar diversity gradient. High
potential energy fluxes characteristic of warm, tropical
regions are speculated to translate into high primary
productivity, which in turn supports complex, speciesrich food webs. In contrast, low potential energy fluxes
characteristic of cool, polar regions are suggested to
translate into low primary productivity, which in turn
supports simple, species-poor food webs. Consistent
with this hypothesis, general climatic variables reflective of environmental energy availability, such as temperature and annual potential evapotranspiration, account for a large proportion (i.e., typically .75%) of
regional variation in species richness (Currie, 1991;
Badgley and Fox, 2000). Recent literature emphasises
the extent to which these general ecological patterns
may correspond to basic temperature-dependent biochemical and metabolic processes (Gaston, 2000; Allen et al., 2002).
The well-studied biogeography of North American
mammals conforms to general species-energy patterns
(Simpson, 1964; Currie, 1991; Badgley and Fox,
2000). The species density of North American mammals in 58,275 km2 quadrats varies from greater than
180 in southern Mexico to less than 20 in the most
northerly continental regions of Canada (Fig. 1; Badgley and Fox, 2000). Five environmental variables, rep-
AND
CLIMATE CHANGE
153
resenting seasonal extremes of temperature, annual energy and moisture, and elevation, account for 88% of
this continental variation in species density (Badgley
and Fox, 2000). Within Canada, mammal species density varies from greater than 80 in southern British
Columbia to less than 10 in the arctic archipelago, and
74% of this variation is explained by mean annual
temperature alone (Fig. 2; Kerr and Packer, 1998).
The species-energy hypothesis provides an empirical basis for predicting the future impacts of climate
change on regional biodiversity (Kerr and Packer,
1998; Currie, 2001). Kerr and Packer (1998) used the
empirical relationship between annual average temperature and mammal species density across Canada
(Fig. 2) to predict how projected climate change might
affect regional mammal diversity. Projected temperature changes over a 75 yr time frame were derived
from the Goddard Institute of Space Science (GISS)
global circulation model (GCM; Russell et al., 1995),
assuming a 1% annual CO2 increase. According to this
and most other GCM’s (e.g., Johns et al., 1997; Boer
et al., 2000; Dai et al., 2001), annual average temperature is expected to increase over the next 75 yrs in
most continental regions of Canada. Based on current
species-energy patterns, Kerr and Packer (1998) predict a corresponding increase in mammal diversity
across Canada, with the largest proportional increases
occurring in far northerly regions where current mammal diversity is lowest and projected temperature increases are greatest (Fig. 3).
Predicted impacts of climate change on biodiversity
derived from current species-energy patterns must be
interpreted with caution. The approach relies on the
assumption that the largely unknown mechanisms
presently linking radiant energy input and species richness will not change in concert with climate (Currie,
2001). Furthermore, the predictions relate only to a
given environment’s potential to support high levels of
diversity, not how realized species richness will vary
over a fixed timeframe. The latter depends critically
on the time lag between environmental change and
biotic responses to that environmental change (Davis,
1986; Malcolm et al., 2002). Finally, the species-energy approach provides no indication of whether potential increases in boreal and arctic diversity will be
realized by the addition of new species to existing
communities or by wholesale community replacement.
Community replacements in proximity to geographical
barriers (e.g., oceans) may leave many northern-adapted species with ‘‘nowhere to go’’ (p. 268; Kerr and
Packer, 1998; Hansell et al., 1998).
Despite the limitations of the species-energy approach in predicting the realized impacts of climate
change on regional biodiversity, it provides an important and robust null expectation. Boreal forests and
arctic tundra are among the coldest and least productive terrestrial environments on earth (Roy et al.,
2001). Climate change projections generally concur
that these regions will undergo unprecedented warming during the next century (Houghton et al., 2001).
154
FIG. 1.
2000).
M. M. HUMPHRIES
ET AL.
Contour map of mammalian species density (number of species per 58,275 km2 quadrat) in North America (from Badgley and Fox,
Global patterns of environmental energy availability,
productivity, and biodiversity indicate that this warming will enhance the potential for increased diversity
in the region (Currie, 1991; Gaston, 2000). As a result,
the environmental impacts of climate change in temperate and polar regions are likely to be shaped by the
appearance of new species at least as much as by the
disappearance of current species.
By what mechanisms will the expected increases in
boreal and arctic mammal diversity occur? Over the
long-term, appearance of new species may result from
speciation and adaptive radiation. But in the shortterm, poleward range expansions of temperate-zone
species will provide the major mechanism by which
boreal and arctic diversity might increase. In the next
section, we describe how energetics can be used to
predict the extent of poleward range expansions for
some mammal species.
II. SEASONAL ENERGETIC BOTTLENECKS AND
RANGE LIMITS
Many mammals routinely experience prolonged,
seasonal periods of negative energy balance when energy requirements exceed energy intake (Robbins,
1993). To survive, individuals must accumulate energy
reserves in advance of the period that are large enough
to support the deficits incurred. Thus, the length and
severity of such seasonal energetic bottlenecks may
serve as a direct constraint on what environments
mammal populations can and cannot occupy. If this is
the case, the considerable complexity normally involved in linking individual energetics to population-
MAMMAL ENERGETICS
FIG. 2. The relationship between contemporary mammal species
richness patterns in Canada and average annual temperature (from
Kerr and Packer, 1998).
level processes (e.g., Moen et al., 1997) becomes reduced to three simple factors; the size of the energy
reserves accumulated prior to the bottleneck, the rate
at which the reserves are depleted during the bottleneck, and the length of the bottleneck. If the size is
less than the rate times the length, individuals cannot
survive the bottleneck and populations will be unable
to persist.
For mammals in boreal and arctic regions, seasonal
energetic bottlenecks typically occur in winter, when
thermoregulatory requirements are elevated and food
resources are scarce. Winter survival requires that sufficient energy can be stored in summer and autumn to
support the energetic deficit accumulated through to
spring. If the energy reserve accumulated prior to the
bottleneck is smaller than the deficit incurred during
the bottleneck, the individual will run out of energy
and die before spring. Some mammals accumulate a
food hoard to support requirements during energetic
bottlenecks (Vander Wall, 1990; Humphries et al.,
2002a), but the majority of mammals rely solely on
body energy reserves. We focus on mammals in the
latter category for the remainder of this section.
Fat is the predominant body energy reserve used by
mammals to fuel metabolism during seasonal bottlenecks. Because lipids yield much more energy per
gram stored than do proteins, mammals rarely maintain non-essential protein reserves (Speakman, 2000).
Thus, the size of fat stores alone provides a good indication of the energy reserves available to an individual. Due either to morphological constraints or costs
associated with fat storage, the maximum size of fat
stores is consistently 40%–50% of total body mass in
both small and large mammals (Millar and Hickling,
1990; Humphries et al., 2003). Given that lipids generate 37.3 kJ energy per gram metabolized, as a rule
of thumb, the maximum amount of energy available
in fat (measured in kJ) at the onset of a seasonal energetic bottleneck will equal 37.3 3 50% of total body
mass (measured in grams), or approximately 19 3 total
body mass. Detailed field studies of pre-bottleneck fat
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155
FIG. 3. Contour map showing percent increases in mammal diversity predicted to occur by 2070 using a species-energy model (from
Kerr and Packer, 1998).
accumulation allow more precise estimates of maximum reserve size for particular species (e.g., Kunz et
al., 1998).
The rate at which fat stores are depleted during energetic bottlenecks depends on resting rates of metabolism, additional costs of thermoregulation, and the
capacity for metabolic depression. Resting metabolism
scales approximately to mass0.75 in mammals, such that
large mammals expend less energy per unit mass than
small mammals. Because fat storage capacity increases
proportionately with body mass (mass1), the fasting
endurance of euthermic mammals generally increases
according to body mass0.25 (Lindstedt and Boyce,
1985; Millar and Hickling, 1990). Thus, while large
mammals can potentially support resting metabolic requirements throughout winter using only fat reserves,
small mammals can support resting requirements with
body fat for less than a month. Furthermore, maintaining a constant, elevated body temperature in winter
requires additional thermoregulatory expenditure beyond resting requirements for most mammal species.
Thermoregulatory requirements are especially high for
small mammals because of their higher lower critical
temperatures and higher thermal conductance, relative
to larger mammals (McNab, 2001). Once thermoregulatory requirements are factored in, the winter fasting
endurance of most small mammals reduces to only a
few days, while that of larger mammals continues to
extend several months. Thus, it is not surprising that
many small mammals (and only a few large mammals)
have evolved the capacity to reversibly enter a state of
metabolic depression that can extend their fasting endurance beyond the length of the seasonal energetic
bottlenecks they experience.
Mammal hibernation provides an especially clear instance where winter survival depends critically on sufficient pre-winter reserve accumulation and where species range limits might be imposed by seasonal energetic bottlenecks. Following termination of activity in
late summer or autumn, most hibernators rely completely on stored fat until spring emergence (Lyman et
al., 1982; French, 1992; Humphries et al., 2003). Fast-
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M. M. HUMPHRIES
FIG. 4. The effect of hibernaculum temperature on total winter energy requirements of Myotis lucifugus (dashed line), based on a winter length of 193 days. The horizontal lines indicate approximate
maximum (solid line) and minimum (dotted line) hibernation fat
stores (from Humphries et al., 2002b).
ing endurance is extended by allowing body temperature to drop to near ambient levels, which reduces
metabolic rate to less than 10% of euthermic levels
(Geiser, 1988; Heldmaier and Ruf, 1992). However,
even when in hibernation, mammals remain constantly
in a metabolically and thermally regulated state, alternating between brief bouts of euthermy, when body
temperatures are regulated at normal, elevated levels,
and prolonged bouts of torpor, when body temperatures are regulated at a much lower torpor set-point
(Lyman et al., 1982; Nedergaard and Cannon, 1990).
Energy requirements when euthermic and torpid, as
well as the frequency of arousals, vary strongly with
ambient temperature.
Recent research on the hibernation energetics and
biogeography of the little brown bat (Myotis lucifugus)
ET AL.
provides an example of how seasonal energetic bottlenecks can limit range distributions and facilitate prediction of range expansions due to climate change
(Humphries et al., 2002b). M. lucifugus is a small
(body mass 6–10 g), insectivorous bat that hibernates
in caves and abandoned mines, relying entirely on
stored body fat during the prolonged winter period
when flying insects are inactive. Integration of the
well-quantified hibernation energetics of this species
reveals that total winter energy requirements vary substantially with winter length and hibernaculum temperature (Humphries et al., 2002b; Fig. 4). Because
relatively simple thermal relationships determine the
length of the hibernation period and the maximum
cave temperatures available for hibernation, both variables can be readily estimated from regional climate
data. Comparison of maximum fat storage capacity
and the projected total hibernation energy requirements of M. lucifugus in different regions of Canada
indicates that this species is excluded from regions
where winters are too long and too cold to permit successful hibernation with maximum fat reserves (Humphries et al., 2002b; Fig. 5). To evaluate how this energetically-imposed range limit would be altered by
future climate change, temperature projections from a
global climate model (Hadley Centre Coupled Model
2 with aerosol simulation mean HadCM2—GAX;
Johns et al., 1997) were used to forecast the energetic
costs of bat hibernation in 2080. In most regions, the
winter range limit of M. lucifugus is expected to move
northward by about 6 km per year over the next eighty
years (Humphries et al., 2002b; Fig. 5).
The energetic bottleneck approach used to predict
the impacts of climate change on the northern range
limits of hibernating bats is equally applicable to the
many other northern mammals that experience season-
FIG. 5. Contemporary and projected M. lucifugus range distributions in northern North America. Confirmed northern hibernacula locations
are indicated with black stars, the contemporary, model-predicted distributional limit of hibernacula is indicated by the solid grey area, and
the 2080 model-predicted distributional limit is indicated by the black and white banded area. The lower margin of grey and banded zones
indicate the limit beyond which to the south almost all bats could successfully hibernate, and the upper margin indicates the limit beyond
which to the north almost no bats could successfully hibernate (redrawn from Humphries et al., 2002b).
MAMMAL ENERGETICS
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CLIMATE CHANGE
157
al energetic bottlenecks. Although parameterization of
the model for M. lucifugus was facilitated by the relatively simple thermal relations that define the duration
of their hibernation period and the hibernaculum temperatures to which they are exposed, the basic logic
and structure of the model applies equally to arctic
ground squirrels (Spermophilus parryii) hibernating on
Alaska’s north slope (Buck and Barnes, 1999a), caribou (Rangifer tarandus) relying on a combination of
foraging and fat reserve depletion to survive on wintering grounds (Russell et al., unpublished), and landlocked polar bears (Ursus maritimus) fasting on the
shores of Hudson Bay during ice-free periods (Derocher et al., 2004). In the final section, we evaluate
the implications of these and other energetic adaptations in a broader, food web context, seeking to predict
the combined outcome of direct and indirect effects of
climate change on energetically differentiated mammal
populations.
III. TROPHIC ENERGY FLOWS
Animal populations are frequently excluded from
potentially suitable habitats by a scarcity of resources
or an abundance of competitors and predators. In these
situations, the impacts of climate change on biogeographic distributions will involve a combination of direct and indirect effects. Trophic energy flow models
provide a useful conceptual approach to predict how
direct effects of climate on one component of a food
web will translate into indirect effects on other components. Because most northern mammals are either
herbivores that feed on plants, or carnivores that feed
on herbivores, their community interactions are reasonably represented by three-link trophic food webs.
We first consider how climate change might alter the
total biomass occupying these three levels via trophic
cascades, before evaluating what functional groups
within a given trophic level may show opposing responses to climate.
IIIa. Trophic cascades and the ecosystem
exploitation hypothesis
According to the hypothesis of exploitation ecosystems (Oksanen et al., 1981; Oksanen and Oksanen,
2000), a combination of low primary productivity and
high endotherm energy requirements severely limits
the number of sustained trophic levels in northern food
webs. At the low end of northern productivity gradients, plant growth occurs to such a limited extent that
no viable herbivore population can be supported (Fig.
6, Zone I). At slightly higher levels of productivity,
herbivores are able to persist but carnivores are not,
and thus herbivores impose strong grazing pressure on
vegetation (Fig. 6, Zone II). At still higher levels of
productivity, carnivores begin to persist and strongly
regulate herbivore densities, thereby releasing vegetation from intense grazing pressure (Fig. 6, Zone III).
Because terrestrial systems generally do not exceed
three trophic levels (terrestrial carnivores specializing
on other terrestrial carnivores are rare), the bracketing
FIG. 6. Biomass of vegetation, herbivores, and carnivores predicted
along a gradient of environmental productivity by Oksanen’s ecosystem exploitation hypothesis (Oksanen et al., 1981; Oksanen and
Oksanen, 2000). Zones I, II, III represent regions expected to be
characterized by one-link, two-link, and three-link trophic dynamics,
respectively. If direct effects of climate on vegetation supersede direct effects on herbivores and carnivores, then responses of most
northern communities to climate change should involve a shift to
the right along the productivity axis.
of herbivore dynamics between vegetation and carnivore regulation may account for the predominance of
plants in terrestrial systems (green world hypothesis,
Hairston et al., 1960). Although there is considerable
disagreement about the actual productivity levels and
geographic localities that conform to the different
zones of Oksanen’s ecosystem exploitation hypothesis
(Oksanen and Oksanen, 2000; Gauthier and Bêty,
2004), the basic hypothesis that primary productivity
plays a major role in trophic organization is widely
accepted.
There is general agreement that summers will become longer, warmer, and wetter throughout most of
northern Canada over the next century (Johns et al.,
1997; Boer et al., 2000; Dai et al., 2001; Houghton et
al., 2001) and that above-ground primary productivity
will increase in accordance with these long-term trends
(Hansell et al., 1998; Aber et al., 2001; Currie, 2001;
Henry, unpublished). In the absence of strongly negative, direct effects of climate change on mammalian
herbivores and carnivores, the population responses of
mammals should be determined primarily by trophic
position as predicted by the ecosystem exploitation hypothesis. Specifically, in response to increased primary
productivity associated with climate change, herbivores should 1) begin to occupy the most productive
zone I regions from which they are currently excluded,
2) increase in abundance in zone II regions where they
currently occur, and 3) maintain similar levels of abundance in zone III regions where carnivores are present
158
M. M. HUMPHRIES
(Fig. 6). Carnivores, on the other hand, should begin
to occupy the most productive zone II regions from
which they are currently excluded (and, as a result,
regulate the herbivore biomass in these regions) and
increase in abundance in zone III regions (Fig. 6).
Strongly negative, or highly divergent, direct effects
of climate change on herbivores and carnivores could
of course impede these anticipated responses. Thus, a
key avenue for future research involves evaluating the
direction and magnitude of climate change’s direct effects on not only individual populations, but also on
trophic levels in aggregate.
At a finer level of resolution, embedded within aggregate trophic-level responses, component populations are likely to respond differentially to climate
change. The response of a given population will depend on the direction and strength of both the direct
and indirect effects influencing its dynamics. For example, caribou (Rangifer tarandus) populations may
decline as a result of climate change, if benefits resulting from increased productivity of plant resources
are overwhelmed by reductions in the accessibility of
resources due to increased depth and hardness of winter snow cover (Caughley and Gunn, 1993). However,
given that direct effects are likely to differ among populations occupying the same trophic level, the decline
of one population may be compensated by population
increases of others. Thus, although caribou may be
negatively impacted by increased snow cover, lemmings (Lemmus, Dicrostonyx spp.) and other small
mammals are likely to be positively impacted (Reid
and Krebs, 1996). The latter populations would therefore experience a triple advantage from a climate
change scenario of increased resource abundance and
increased snow cover—more resources, better access
to resources, and reduced competition from populations negatively impacted by snow cover—and can be
expected to increase in abundance as a result. Thus,
while it is clearly critical to consider the possibility of
direct, population-specific effects when making community-level predictions, it is equally important that
the ramifications of population-specific effects be considered within their broader trophic context. Frequently what is bad for one population will tend to be good
for another. Thus, a second key avenue for future research involves identification of different functional
groups within trophic categories that will exhibit opposing population responses to climate change. We
identify one such functional group classification in the
next section.
IIIb. Apparent competition and coexistence along a
continuum of seasonal strategies
Boreal and arctic ecosystems are characterized by
short summer pulses of primary productivity, interspersed by prolonged winter periods of cold temperatures and vegetation senescence or growth arrest.
Northern winters are a major energetic challenge for
endotherms because snow cover and low ambient temperatures simultaneously reduce resource availability
ET AL.
and elevate resource requirements (King and Murphy,
1985; Davenport, 1992; Robbins, 1993; Speakman,
2000). Endotherm adaptations to the resulting seasonal
energetic bottleneck include anticipatory energy storage (Humphries et al., 2003), increased insulation
(Scholander et al., 1950; McNab, 2001), refuge occupation (Huey, 1991), torpor expression (Lyman et
al., 1982) and migration (Dingle, 1996).
Differential expression of seasonal energetic adaptations generates a continuum in the trophic status of
endotherms during winter. At one extreme are species
that avoid the bottleneck via hibernation in refuges
(temporal avoidance) or migration out of the region
(spatial avoidance), and thus completely decouple
from the food web during winter. Because terrestrial
mammals are either non-migratory or do not migrate
sufficient distances to truly decouple from seasonal environments (Dingle, 1996), and because migration introduces the added complexity of allochthonous energy inputs into local systems (Jefferies and Rockwell,
2004), we limit our consideration here to mammals
expressing in situ winter inactivity. We refer to these
species as seasonal. At the other extreme of the seasonality continuum, are species that simply tolerate the
bottleneck, and thus exhibit unchanged or even increased resource consumption and predator susceptibility during winter. We refer to these species as continuous. Populations occupying different positions
along this continuum should be differentially affected
by the moderated seasonality that climate change will
introduce to northern food webs.
Because winters become increasingly severe at
higher latitudes, seasonal strategies might be expected
to predominate among the mammals present in the far
north. To test this prediction, we considered all herbivorous mammal species occupying the Deciduan,
Coniferan, and Tundran subregions of North America
as delineated by Hagmeier (1966). Using Banfield
(1974) and Wilson and Ruff (1999), we qualitatively
ranked the extent to which each of these species decouple from resources and predators during winter.
The lowest seasonality rank (SR 5 1) was assigned to
species characterized by no significant declines in resource consumption and predator susceptibility during
winter (e.g., hares and ungulates). The highest rank
(SR 5 4) was reserved for species with substantial prewinter energy storage, greatly reduced predator susceptibility during winter, and a capacity to substantially depress metabolism via torpor expression (e.g.,
ground squirrels and chipmunks). Intermediate ranks
were applied to species with small to moderate reductions in either resource consumption or predator susceptibility during winter (SR 5 2; e.g., lemmings and
red squirrels) or with small to moderate reductions in
both (SR 5 3; e.g., beaver and pika).
In contrast to the prediction that seasonal energetic
strategies will predominate where winter conditions
are harshest, seasonal mammalian herbivores are more
common in southern and central North America than
in northern North America. Highly seasonal species
MAMMAL ENERGETICS
TABLE 1. Species diversity of continuous and seasonal mammal
herbivores in three subregions of North America.
Mammal
Subregion
Total
Continuous
Seasonal
Proportion
Seasonal
(%)
Deciduan
Coniferan
Tundran
73
88
14
50
56
13
23
32
1
32
36
7
Mammal Herbivore Species
(SR 5 3 or 4) account for approximately one third of
Deciduan and Coniferan mammals but less than 10%
of Tundran mammals (Table 1). The only highly seasonal mammal occupying tundra communities is the
Arctic ground squirrel (Spermophilus parryii; SR 5 4),
and even this species occurs only in the southern portion of the Tundran subregion. Accordingly, highly
seasonal mammals form a major component of mammalian herbivore communities in boreal forests, but
are entirely absent from high arctic communities (Table 2). Migratory birds and diapausing insects are present throughout the arctic (Gauthier and Bêty, 2004;
Danks, 2004), and thus overall herbivory in arctic systems may remain highly seasonal. However, for mammals, which are unable to migrate as far as birds or
develop as rapidly as insects, high arctic summers are
apparently too short and winters too long for a seasonal strategy to be viable.
Seasonal mammals may be absent from the far north
because of purely abiotic limitations or because of
competitive exclusion by continuous species. In Section II, we identify a situation where the northern
range limit of a seasonal species (Myotis lucifugus)
appears to be imposed by abiotic constraints involving
an interaction between maximum autumn energy reserves and minimum winter energy requirements. Permafrost barriers to subterranean thermal refugia may
represent an additional constraint on subterranean hibernators in the arctic (Buck and Barnes, 1999b). Conversely, seasonal species may be excluded from otherwise suitable habitats by the presence of continuous
competitors that suppress their resources and support
populations of shared predators (Holt and Lawton,
TABLE 2.
Location
Ellef Ringnes, Nunavut (788N, 1028W)
Kluane, Yukon (618N, 1388W)2
1
2
Krebs et al., 2003.
Krebs et al., 2001.
CLIMATE CHANGE
159
1994). Competition between seasonal and continuous
species is a key consideration even in the case of abiotic exclusion of seasonal species, because if climate
change were to eliminate or weaken the abiotic constraint, then competition outcomes with continuous
herbivores would become the key determinant of the
invasibility of seasonal populations.
For seasonal and continuous herbivores to coexist
under resource competition and shared predation from
carnivores, the relative competitive advantage of the
two strategies must reverse with season (Namba, 1984;
Chesson, 2000). This trade-off could be structured in
one of two ways. Relative to continuous herbivores,
seasonal herbivores could experience greater biomass
increases during summer (because of higher maximum
consumption rates, higher reproductive output, and/or
lower predation rates) and greater losses during winter
(because of fasting and/or higher winter mortality).
Conversely, seasonal herbivores could experience lesser biomass increases during summer (because of lower
maximum consumption rates, lower reproductive output, or higher predation rates) and lesser losses during
winter (because of lower energetic costs or lower predation rates). Whichever population experiences a relative competitive advantage during summer (i.e.,
growth maximizers) should be characterized by greater
seasonal fluctuations than the population garnering a
competitive advantage during winter (i.e., loss minimizers).
Although either form of this seasonality trade-off is
sufficient to maintain long-term coexistence in a seasonal environment, the distinction is critical because it
will determine how continuous and seasonal species
will respond to climate change. Whichever strategy
currently garners a competitive advantage during summer (i.e., is characterized by a proportionately higher
spring to autumn biomass increase) will benefit from
the longer and warmer summers projected to occur in
the future, at the expense of the strategy currently garnering a competitive advantage during winter (i.e.,
characterized by proportionately lower autumn to
spring biomass decreases). Thus, if seasonal species
currently undergo more pronounced seasonal fluctua-
Herbivore composition of northern mammal communities.
Predominant Mammalian Herbivores
1
Banks Island, NWT (728N, 1238W)1
AND
Caribou (Rangifer tarandus)
Lemming (Dicrostonyx groenlandicus)
Muskox (Ovibos moschatus)
Lemming (Dicrostonyx groenlandicus, Lemmus sibiricus)
Caribou (Rangifer tarandus)
Arctic hare (Lepus arcticus)
Snowshoe hare (Lepus americanus)
Arctic ground squirrel (Spermophilus parryii)
Red squirrel (Tamiasciurus hudsonicus)
Moose (Alces alces)
Seasonality
Rank
Approximate
Biomass
(kg/km2)
1
2
1
2
1
1
1
4
2
1
77
,1
330
8
6
,1
160
58
57
40
160
M. M. HUMPHRIES
FIG. 7. Biomass of vegetation, carnivores, continuous herbivores,
and seasonal herbivores predicted along a gradient of environmental
productivity. Predictions are derived from Oksanen’s ecosystem exploitation hypothesis (Oksanen et al., 1981; Oksanen and Oksanen,
2000) and contemporary distributions of seasonal and continuous
herbivores (Table 1). Zones I, II, III represent regions expected to
be characterized by one-link, two-link, and three-link trophic dynamics, respectively. Zone III is further subdivided into regions
without (IIIa) and with (IIIb) seasonal herbivores. If direct effects
of climate on vegetation supersede direct effects on herbivores and
carnivores, then responses of most northern communities to climate
change should involve a shift to the right along the productivity axis.
tions in biomass than continuous species do, then seasonal populations should increase in response to climate change while continuous populations decline.
This prediction should hold even if continuous and
seasonal herbivores are characterized by less than
complete dietary overlap, so long as climate change
effects on the duration of seasons are not perfectly
confounded by differential climate change responses
of their respective plant resources (Grover, 1995).
Current latitudinal distributions of seasonal and continuous mammals suggest that seasonal species will
benefit most from climate warming. Given that seasonal mammals currently occur everywhere in northern North America except for the regions characterized
by the longest winters and shortest summers, seasonal
species appear either to be abiotically excluded from
northern environments or to garner a competitive advantage relative to continuous species as a result of
longer summers and shorter winters. Thus, in the future, as northern Coniferan and southern Tundran summers lengthen and winters shorten, we can expect a
shift in the relative competitive advantage of the two
strategies, with seasonal herbivores increasing in abundance in regions where they currently occur (Fig. 7,
Zone IIIb) and expanding their ranges into regions
where they are currently excluded (Fig. 7, Zone IIIa).
Modifying Oksanen’s productivity zones to incor-
ET AL.
porate the functional distinction between seasonal and
continuous species, continuous herbivores are the first
mammals to appear along a north-to-south (low-tohigh) productivity gradient, followed by continuous
carnivores, followed by seasonal herbivores (Fig. 7).
Zone IIIa of Figure 7 is thus representative of vast
regions of the Canadian arctic where resident carnivores (e.g., arctic foxes and wolves) have an important
influence on continuous herbivore dynamics, and
where seasonal mammal herbivores are absent (Gauthier and Bêty, 2004; Krebs et al., 2003). Zone IIIb of
Figure 7 is representative of many other regions of
northern North America where continuous and seasonal herbivores coexist under shared predation from continuous carnivores.
Concomitant with the predicted northward spread of
seasonal herbivores due to climate change, continuous
herbivores already present in the Canadian arctic are
likely to experience population declines for several
reasons. First, increased summer length will reduce the
proportion of the annual cycle during which continuous species experience a relative competitive advantage over seasonal species. Second, increased primary
productivity will be monopolized by seasonal species
that are at a competitive advantage in summer when
vegetation growth occurs. Third, increased carnivore
biomass, resulting from productivity cascades, will
have disproportionate top-down control on continuous
herbivores because their seasonal competitors become
unavailable to predators during winter. This latter outcome reflects an important cryptic benefit of a seasonal
energetic strategy. Although evaluation of the advantages of hibernation are often limited to energetic considerations (Humphries et al., 2003), the capacity for
a population to avoid supporting its predators for prolonged seasonal periods and to transfer this burden to
its competitors, may represent a major ecological benefit of hibernation.
Before concluding, we briefly consider the seasonality of mammalian carnivores along the North-South
productivity gradient. The few mammalian carnivores
present in northern systems (e.g., wolf, foxes, lynx,
wolverine, weasels) tend to be continuously active,
whereas several carnivores limited to more southerly
regions are seasonally inactive (e.g., badger, skunks,
racoons). Canids and, to a lesser extent, felids are present in the Tundran, Coniferan, and Deciduan subregions always as continuous carnivores. All Tundran
and northern Coniferan mustelids are active throughout winter (e.g., wolverine, Gulo gulo; fisher and marten, Martes spp.; weasels and mink, Mustela spp.),
whereas several mustelids present in the southern Coniferan and throughout the Deciduan are characterized
by varying extents of winter dormancy (badger, Taxidea taxus; skunks, Mephitis spp., Conepatus leuconotus, Spilogale putorius). The occurrence of hibernating grizzly bears (Ursus arctos) in southern Tundran
regions is a partial exception to this carnivore trend,
but even within North American bears the general pattern holds, with the most northerly species (polar bear,
MAMMAL ENERGETICS
Ursus maritimus) characterized by less seasonality
than its southern congenerics (U. arctos, U. americanus). Thus, the northern range limits of seasonal carnivores may result from similar abiotic or biotic constraints affecting seasonal herbivores, albeit at different thresholds of seasonality and productivity.
SUMMARY
The causes and projected consequences of global
climate change are not yet fully resolved, and it remains unclear how animal populations will be affected
by even the most robust and widely accepted components of projected climate change. Although mammals
are characterized by extraordinarily wide thermal tolerance and possess highly specialized adaptations for
dealing with seasonal temperature variation, they, like
all animals, remain fundamentally affected by temperature. Given that climate change will substantially alter
ambient temperature patterns in northern regions, as
well as change many other components of the abiotic
(e.g., precipitation, snow and ice cover) and biotic environment (e.g., abundance and distribution of resources and predators), the mammal fauna of northern Canada is likely to undergo major changes during the next
century.
Additional data and better theory are needed to reliably predict the direction and magnitude of climate
change impacts on specific mammal species. In this
review, we have therefore attempted only to illustrate
how bioenergetic approaches relate to climate change
impacts at various levels of resolution (e.g., regional
diversity, species range extensions, trophic interactions) and to generate hypotheses that might motivate
additional research. Further progress in predicting the
impacts of climate change on northern mammals
awaits integration of the conceptual approaches outlined in this review with detailed field studies of specific northern communities. Thus, rather than concluding with speculative predictions about possible impacts
of climate change on particular northern mammals, we
conclude with four general points that are central to,
and have emerged from, the bioenergetic approaches
we employed:
1. Current global patterns of energy availability, productivity, and biodiversity suggest that the impacts
of climate change in temperate and polar regions
will be shaped by the appearance of new species at
least as much as by the disappearance of current
species.
2. Because climate change will produce change at
multiple levels of biological organization, prediction of its impacts on mammals need to be extended
beyond consideration of individual populations or
species, to the functional groups and trophic categories that comprise biological communities.
3. Bioenergetic approaches are ideally suited to predicting the impacts of climate change at multiple
levels of organization because energy budgets integrate biotic and abiotic influences and translate
AND
CLIMATE CHANGE
161
individual animal function into population and
community outcomes.
4. Seasonality is a fundamental property of northern
systems with major effects on all biotic components. A key consideration in the prediction of climate change impacts on northern mammals thus involves how mammal energetics and trophic dynamics vary with season and how seasonality will be
altered by climate change.
REFERENCES
Aber, J., R. P. Neilson, S. McNulty, J. M. Lenihan, D. Bechelet, and
R. J. Drapek. 2001. Forest processes and environmental change:
predicting the effects of individual and multiple stressors.
BioScience 51:735–751.
Allen, A. P., J. H. Brown, and J. F. Gillooly. 2002. Global biodiversity, biochemical kinetics, and the energetic-equivalence rule.
Science 297:1545–1548.
Badgley, C. and D. L. Fox. 2000. Ecological biogeography of North
American mammals: Species density and ecological structure in
relation to environmental gradients. J. Biogeogr. 27:1437–1467.
Banfield, A. W. F. 1974. The mammals of Canada. University of
Toronto Press, Toronto.
Boer, G. J., G. M. Flato, and D. Ramsden. 2000. A transient climate
change simulation with greenhouse gas and aerosol forcing:
Projected climate change to the 21st century. Climate Dyn. 16:
427–450.
Buck, C. L. and B. M. Barnes. 1999a. Annual cycle of body composition and hibernation in free-living arctic ground squirrels.
J. Mamm. 80:430–442.
Buck, C. L. and B. M. Barnes. 1999b. Temperatures of hibernacula
and changes in body composition of arctic ground squirrels over
winter. J. Mamm. 80:1264–1276.
Caughley, G. and A. Gunn. 1993. Dynamics of large herbivores in
deserts: Kangaroos and caribou. Oikos 67:47–55.
Chesson, P. 2000. Mechanisms of maintenance of species diversity.
Annu. Rev. Ecol. Syst. 31:343–366.
Currie, D. J. 1991. Energy and large-scale patterns of animal- and
plant-species richness. Am. Nat. 137:27–49.
Currie, D. J. 2001. Projected effects of climate change on patterns
of vertebrate and tree species richness in the conterminous United States. Ecosystems 4:216–225.
Dai, A., T. M. L. Wigley, B. A. Boville, J. T. Kiehl, and L. E. Buja.
2001. Climates of the twentieth and twenty-first centuries simulated by the NCAR climate system model. J. Climate 14:485–
519.
Danks, H. V. 2004. Seasonal adaptations in arctic insects. Integr.
Comp. Biol. 44:85–94.
Davenport, J. 1992. Animal life at low temperature. Chapman and
Hall, London.
Davis, M. B. 1986. Climatic instability, time lags, and community
disequilibrium. In J. Diamond and T. J. Case (eds.), Community
ecology, pp. 269–284. Harper & Row, New York.
Derocher A. E., N. J. Lunn, I. Stirling. 2004. Polar bears in a warming climate. Integr. Comp. Biol. 44:163–176.
Dingle, H. 1996. Migration: The biology of life on the move. Oxford
University Press, New York.
French, A. R. 1992. Mammalian dormancy. In T. E. Tomasi and T.
H. Horton (eds.), Mammalian energetics, pp. 105–131. Comstock Publishing, Ithaca, N.Y.
Gaston, K. J. 2000. Global patterns in biodiversity. Nature 405:220–
227.
Gauthier, G., J. Bêty, J.-F. Giroux, L. Rochefort. 2004. Trophic
interactions in a high Arctic snow goose colony. Integr. Comp.
Biol. 44:119–129.
Geiser, F. 1988. Reduction of metabolism during hibernation and
daily torpor in birds and mammals: Temperature effect or physiological inhibition? J. Comp. Physiol. 158:25–38.
Grover, J. P. 1995. Competition, herbivory, and enrichment: Nutri-
162
M. M. HUMPHRIES
ent-based models for edible and inedible plants. Am. Nat. 145:
746–774.
Hagmeier, E. M. 1966. A numerical analysis of the distributional
patterns of North American mammals. II. Re-evaluation of the
provinces. Syst. Zool. 15:279–299.
Hairston, N. G., F. E. Smith, and L. B. Slobodkin. 1960. Community
structure, population control, and competition. Am. Nat. 94:
421–425.
Hansell, R. I. C., J. R. Malcolm, H. Welch, R. L. Jefferies, and P.
A. Scott. 1998. Atmospheric change and biodiversity in the Arctic. Environ. Monit. Assess. 49:303–325.
Heldmaier, G. and T. Ruf. 1992. Body temperature and metabolic
rate during natural hypothermia in endotherms. J. Comp. Physiol. B 158:696–706.
Holt, R. D. and J. H. Lawton. 1994. The ecological consequences
of shared natural enemies. Annu. Rev. Ecol. Syst. 25:495–520.
Houghton, J. T., Y. Ding, D. J. Griggs, M. Noguer, P. J. van der
Linden, X. Dai, K. Maskell, and C. A. Johnson. (eds.) 2001.
Climate change 2001. The scientific basis. Contribution of
Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University
Press, Cambridge.
Huey, R. B. 1991. Physiological consequences of habitat selection.
Am. Nat. 137:S91–S115.
Humphries, M. M., D. W. Thomas, C. L. Hall, J. R. Speakman, and
D. L. Kramer. 2002a. The energetics of autumn mast hoarding
in eastern chipmunks. Oecologia 133:30–37.
Humphries, M. M., D. W. Thomas, and J. R. Speakman. 2002b.
Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418:313–316.
Humphries, M. M., D. W. Thomas, and D. L. Kramer. 2003. The
role of energy availability in mammalian hibernation: A cost
benefit approach. Physiol. Biochem. Zool. 76:165–179.
Jefferies, R. L., R. F. Rockwell, and K. F. Abraham. 2004. Agricultural food subsidies, migratory connectivity and large-scale disturbance in Arctic coastal systems: A case study. Integr. Comp.
Biol. 44:130–139.
Johns, T. C., R. E. Carnell, J. F. Crossley, J. M. Gregory, J. F. B.
Mitchell, C. A. Senior, S. F. B. Tett, and R. A. Wood. 1997.
The second Hadley Centre coupled ocean-atmosphere GCM:
Model description, spinup and validation. Climate Dyn. 13:103–
134.
Kerr, J. and L. Packer. 1998. The impact of climate change on mammal diversity in Canada. Environ. Monit. Assess. 49:263–270.
King, J. R. and M. E. Murphy. 1985. Periods of nutritional stress in
the annual cycles of endotherms: fact or fiction? Amer. Zool.
25:955–964.
Krebs, C. J., S. Boutin, and R. Boonstra. 2001. Ecosystem dynamics
of the boreal forest: The Kluane project. Oxford University
Press, New York.
Krebs, C. J., K. Danell, A. Angerbjörn, J. Agrell, D. Berteaux, K.
A. Bråthen, Ö Danell, S. Erlinge, V. Fedorov, K. Fredga, J.
Hjältén, G. Högstdedt, I. S. Jónsdóttir, A. J. Kenney, N. Kjellén,
T. Nordin, H. Roininen, M. Svensson, M. Tannerfeldt, and C.
Wiklund. 2003. Terrestrial trophic dynamics in the Canadian
Arctic. Can. J. Zool. 81:827–843.
Kunz, T. H., J. A. Wrazen, and C. D. Burnett. 1998. Changes in
ET AL.
body mass and fat reserves in pre-hibernating little brown bats
(Myotis lucifugus). Ecoscience 5:8–17.
Lindstedt, S. L. and M. S. Boyce. 1985. Seasonality, fasting endurance, and body size in mammals. Am. Nat. 125:873–878.
Ludwig, D., M. Mangel, and B. Haddad. 2001. Ecology, conservation, and public policy. Annu. Rev. Ecol. Syst. 32:481–517.
Lyman, C. P., J. S. Willis, A. Malan, and L. C. H. Wang. 1982.
Hibernation and torpor in mammals and birds. Academic Press,
New York.
MacArthur, R. H. 1965. Patterns of species diversity. Biol. Rev.
Camb. Philos. Soc. 40:510–533.
Malcolm, J. R., A. Markham, R. P. Neilson, and M. Garaci. 2002.
Estimated migration rates under scenarios of global climate
change. J. Biogeogr. 29:835–849.
McNab, B. K. 2001. The physiological ecology of vertebrates: A
view from energetics. Cornell University Press, Cornell.
Millar, J. S. and G. J. Hickling. 1990. Fasting endurance and the
evolution of mammalian body size. Funct. Ecol. 4:5–12.
Moen, R., J. Pastor, and Y. Cohen. 1997. A spatially explicit model
of moose foraging and energetics. Ecology 78:505–521.
Namba, T. 1984. Competitive coexistence in a seasonally fluctuating
environment. J. Theor. Biol. 111:369–386.
Nedergaard, J. and B. Cannon. 1990. Mammalian hibernation. Philos. Trans. R. Soc. London B Biol. Sci. 326:669–686.
Odum, E. 1963. Ecology. Holt, Rinehart & Winston. New York.
Oksanen, L. and T. Oksanen. 2000. The logic and realism of the
hypothesis of exploitation ecosystems. Am. Nat. 155:703–723.
Oksanen, L., S. D. Fretwell, J. Arruda, and P. Niemelä. 1981. Exploitation ecosystems in gradients of primary productivity. Am.
Nat. 118:240–261.
Parmesan, C. and G. Yohe. 2003. A globally coherent fingerprint of
climate change impacts across natural systems. Nature 421:37–
42.
Reid, D. G. and C. J. Krebs. 1996. Limitations to collared lemming
population growth in winter. Can. J. Zool. 74:1284–1291.
Robbins C. T. 1993. Wildlife feeding and nutrition. Academic Press,
Inc., San Diego, Calif.
Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rosenzweig,
and J. A. Pounds. 2003. Fingerprints of global warming on wild
animals and plants. Nature 421:57–60.
Rosenzweig, M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge.
Roy, J., B. Saugier, and H. A. Mooney. (eds.) 2001. Terrestrial global productivity. Academic Press, San Diego.
Russell, G. L., J. R. Miller, and D. Rind. 1995. A coupled atmosphere-ocean model for transient climate change studies. Atmos.
Ocean 33:683–730.
Scholander, P. F., V. Waters, R. Hock, and L. Irving. 1950. Body
insulation of some arctic and tropical mammals and birds. Biol.
Bull. 99:225–235.
Simpson, G. G. 1964. Species density of North American Recent
mammals. Syst. Zool. 13:57–73.
Speakman, J. R. 2000. The cost of living: Field metabolic rates of
small mammals. Adv. Ecol. Res. 30:177–297.
Vander Wall, S. B. 1990. Food hoarding in animals. University of
Chicago Press, Chicago.
Wilson, D. E. and S. Ruff. 1999. Smithsonian book of North American mammals. Smithsonian Institute Press, Washington.
Yodzis, P. and S. Innes. 1992. Body size and consumer-resource
dynamics. Am. Nat. 139:1151–1175.